Skip to main content

Advertisement

SpringerLink
Log in

Insights into Craniofacial Development and Anomalies: Exploring Fgf Signaling in Zebrafish Models

  • REVIEW
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

To illustrate the value of using zebrafish to understand the role of the Fgf signaling pathway during craniofacial skeletal development under normal and pathological conditions.

Recent Findings

Recent data obtained from studies on zebrafish have demonstrated the genetic redundancy of Fgf signaling pathway and have identified new molecular partners of this signaling during the early stages of craniofacial skeletal development.

Summary

Studies on zebrafish models demonstrate the involvement of the Fgf signaling pathway at every stage of craniofacial development. They particularly emphasize the central role of Fgf signaling pathway during the early stages of the development, which significantly impacts the formation of the various structures making up the craniofacial skeleton. This partly explains the craniofacial abnormalities observed in disorders associated with FGF signaling. Future research efforts should focus on investigating zebrafish Fgf signaling during more advanced stages, notably by establishing zebrafish models expressing mutations responsible for diseases such as craniosynostoses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Ornitz DM, Itoh N. The Fibroblast Growth Factor signaling pathway. Wiley Interdiscip Rev Dev Biol. 2015;4:215–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Xie Y, Su N, Yang J, Tan Q, Huang S, Jin M, et al. FGF/FGFR signaling in health and disease. Sig Transduct Target Ther. 2020;5:181.

    Article  CAS  Google Scholar 

  3. Ornitz DM, Itoh N. New developments in the biology of fibroblast growth factors. WIREs Mechanisms of Disease. 2022;14: e1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Dambroise E, Ktorza I, Brombin A, Abdessalem G, Edouard J, Luka M, et al. Fgfr3 is a positive regulator of osteoblast expansion and differentiation during zebrafish skull vault development. J Bone Miner Res. 2020. Role of Fgfr3 during cranial vault development

  5. Maves L, Jackman W, Kimmel CB. FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development. 2002;129:3825–37.

    Article  CAS  PubMed  Google Scholar 

  6. Liu K, Lv Z, Huang H, Yu S, Xiao L, Li X, et al. FGF3 from the Hypothalamus Regulates the Guidance of Thalamocortical Axons. Dev Neurosci. 2020;42:208–16.

    Article  PubMed  Google Scholar 

  7. Grillo L, Greco D, Pettinato R, Avola E, Potenza N, Castiglia L, et al. Increased FGF3 and FGF4 gene dosage is a risk factor for craniosynostosis. Gene. 2014;534:435–9.

    Article  CAS  PubMed  Google Scholar 

  8. Zhang Y-B, Hu J, Zhang J, Zhou X, Li X, Gu C, et al. Genome-wide association study identifies multiple susceptibility loci for craniofacial microsomia. Nat Commun. 2016;7:10605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jackman WR, Draper BW, Stock DW. Fgf signaling is required for zebrafish tooth development. Dev Biol. 2004;274:139–57.

    Article  CAS  PubMed  Google Scholar 

  10. Choe CP, Crump JG. Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a. Development. 2014;141:3583–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kesavan G, Raible F, Gupta M, Machate A, Yilmaz D, Brand M. Isthmin1, a secreted signaling protein, acts downstream of diverse embryonic patterning centers in development. Cell Tissue Res. 2021;383:987–1002.

    Article  CAS  PubMed  Google Scholar 

  12. Walshe J, Mason I. Unique and combinatorial functions of Fgf3 and Fgf8 during zebrafish forebrain development. Development. 2003;130:4337–49.

    Article  CAS  PubMed  Google Scholar 

  13. Albertson RC, Yelick PC. Fgf8 haploinsufficiency results in distinct craniofacial defects in adult zebrafish. Dev Biol. 2007;306:505–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gebuijs IGE, Raterman ST, Metz JR, Swanenberg L, Zethof J, Van Den Bos R, et al. Fgf8a mutation affects craniofacial development and skeletal gene expression in zebrafish larvae. Biology Open. 2019;bio.039834. https://doi.org/10.1242/bio.039834.

  15. Xu H, Niu Y, Wang T, Liu S, Xu H, Wang S, et al. Novel FGFR1 and KISS1R Mutations in Chinese Kallmann Syndrome Males with Cleft Lip/Palate. Biomed Res Int. 2015;2015:1–9.

    CAS  Google Scholar 

  16. Rodriguez-Zabala M, Aza-Carmona M, Rivera-Pedroza CI, Belinchón A, Guerrero-Zapata I, Barraza-García J, et al. FGF9 mutation causes craniosynostosis along with multiple synostoses. Hum Mutat. 2017;38:1471–6.

    Article  CAS  PubMed  Google Scholar 

  17. He X, Yan Y-L, Eberhart JK, Herpin A, Wagner TU, Schartl M, et al. miR-196 regulates axial patterning and pectoral appendage initiation. Dev Biol. 2011;357:463–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Swartz ME, Sheehan-Rooney K, Dixon MJ, Eberhart JK. Examination of a palatogenic gene program in zebrafish. Dev Dyn. 2011;240:2204–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jovelin R, Yan Y-L, He X, Catchen J, Amores A, Canestro C, et al. Evolution of developmental regulation in the vertebrate FgfD subfamily. J Exp Zool B Mol Dev Evol. 2010;314:33–56.

    Article  PubMed  PubMed Central  Google Scholar 

  20. FGF17 - an overview | ScienceDirect Topics [Internet]. [cited 2024 Feb 15]. Available from: https://www.sciencedirect.com/topics/biochemistry-genetics-and-molecular-biology/fgf17.

  21. Nomura R, Kamei E, Hotta Y, Konishi M, Miyake A, Itoh N. Fgf16 is essential for pectoral fin bud formation in zebrafish. Biochem Biophys Res Commun. 2006;347:340–6.

    Article  CAS  PubMed  Google Scholar 

  22. ZFIN Publication: Thisse et al., 2005 [Internet]. [cited 2024 Feb 15]. Available from: https://zfin.org/ZDB-PUB-051025-1.

  23. Cooper WJ, Wirgau RM, Sweet EM, Albertson RC. Deficiency of zebrafish fgf20a results in aberrant skull remodeling that mimics both human cranial disease and evolutionarily important fish skull morphologies. Evol Dev. 2013;15:426–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mitchell JM, Sucharov J, Pulvino AT, Brooks EP, Gillen AE, Nichols JT. The alx3 gene shapes the zebrafish neurocranium by regulating frontonasal neural crest cell differentiation timing. Development. 2021;148:dev197483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yamauchi H, Goto M, Katayama M, Miyake A, Itoh N. Fgf20b is required for the ectomesenchymal fate establishment of cranial neural crest cells in zebrafish. Biochem Biophys Res Commun. 2011;409:705–10.

    Article  CAS  PubMed  Google Scholar 

  26. Sugimoto K, Hui SP, Sheng DZ, Kikuchi K. Dissection of zebrafish shha function using site-specific targeting with a Cre-dependent genetic switch. Elife. 2017;6: e24635.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Rothenbuhler A, Fadel N, Debza Y, Bacchetta J, Diallo MT, Adamsbaum C, et al. High Incidence of Cranial Synostosis and Chiari I Malformation in Children With X-Linked Hypophosphatemic Rickets (XLHR). J Bone Miner Res. 2018

  28. Larbuisson A, Dalcq J, Martial JA, Muller M. Fgf receptors Fgfr1a and Fgfr2 control the function of pharyngeal endoderm in late cranial cartilage development. Differentiation. 2013;86:192–206.

    Article  CAS  PubMed  Google Scholar 

  29. Koch P, Löhr HB, Driever W. A mutation in cnot8, component of the Ccr4-not complex regulating transcript stability, affects expression levels of developmental regulators and reveals a role of Fgf3 in development of caudal hypothalamic dopaminergic neurons. PLoS ONE. 2014;9: e113829.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rohs P, Ebert AM, Zuba A, McFarlane S. Neuronal expression of fibroblast growth factor receptors in zebrafish. Gene Expr Patterns. 2013;13:354–61.

    Article  CAS  PubMed  Google Scholar 

  31. Topczewska JM, Shoela RA, Tomaszewski JP, Mirmira RB, Gosain AK. The Morphogenesis of Cranial Sutures in Zebrafish. PLoS ONE. 2016;11: e0165775.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Schell U, Hehr A, Feldman GJ, Robin NH, Zackai EH, de Die-Smulders C, et al. Mutations in FGFR1 and FGFR2 cause familial and sporadic Pfeiffer syndrome. Hum Mol Genet. 1995;4:323–8.

    Article  CAS  PubMed  Google Scholar 

  33. Farrow EG, Davis SI, Mooney SD, Beighton P, Mascarenhas L, Gutierrez YR, et al. Extended mutational analyses of FGFR1 in osteoglophonic dysplasia. Am J Med Genet A. 2006;140:537–9.

    Article  PubMed  Google Scholar 

  34. Duszynski RJ, Topczewski J, LeClair EE. Divergent requirements for fibroblast growth factor signaling in zebrafish maxillary barbel and caudal fin regeneration. Dev Growth Differ. 2013;55:282–300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. ZFIN Publication: Thisse et al., 2008 [Internet]. [cited 2024 Feb 15]. Available from: https://zfin.org/ZDB-PUB-080227-22.

  36. Paudel S, Gjorcheska S, Bump P, Barske L. Patterning of cartilaginous condensations in the developing facial skeleton. Developmental Biology. 2022;486:44–55. https://doi.org/10.1016/j.ydbio.2022.03.010. Involvement of FGF signaling in PCC formation.

  37. Wilkie AO, Slaney SF, Oldridge M, Poole MD, Ashworth GJ, Hockley AD, et al. Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome. Nat Genet. 1995;9:165–72.

    Article  CAS  PubMed  Google Scholar 

  38. Reardon W, Winter RM, Rutland P, Pulleyn LJ, Jones BM, Malcolm S. Mutations in the fibroblast growth factor receptor 2 gene cause Crouzon syndrome. Nat Genet. 1994;8:98–103.

    Article  CAS  PubMed  Google Scholar 

  39. Ibrahimi OA, Zhang F, Eliseenkova AV, Linhardt RJ, Mohammadi M. Proline to arginine mutations in FGF receptors 1 and 3 result in Pfeiffer and Muenke craniosynostosis syndromes through enhancement of FGF binding affinity. Hum Mol Genet. 2004;13:69–78.

    Article  CAS  PubMed  Google Scholar 

  40. Fonseca R, Costa-Lima MA, Cosentino V, Orioli IM. Second case of Beare-Stevenson syndrome with an FGFR2 Ser372Cys mutation. Am J Med Genet A. 2008;146A:658–60.

    Article  CAS  PubMed  Google Scholar 

  41. Przylepa KA, Paznekas W, Zhang M, Golabi M, Bias W, Bamshad MJ, et al. Fibroblast growth factor receptor 2 mutations in Beare-Stevenson cutis gyrata syndrome. Nat Genet. 1996;13:492–4.

    Article  CAS  PubMed  Google Scholar 

  42. Ledwon JK, Turin SY, Gosain AK, Topczewska JM. The expression of fgfr3 in the zebrafish head. Gene Expr Patterns. 2018;29:32–8.

    Article  CAS  PubMed  Google Scholar 

  43. Rousseau F, Bonaventure J, Legeai-Mallet L, Pelet A, Rozet JM, Maroteaux P, et al. Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature. 1994;371:252–4.

    Article  CAS  PubMed  Google Scholar 

  44. Bellus GA, McIntosh I, Smith EA, Aylsworth AS, Kaitila I, Horton WA, et al. A recurrent mutation in the tyrosine kinase domain of fibroblast growth factor receptor 3 causes hypochondroplasia. Nat Genet. 1995;10:357–9.

    Article  CAS  PubMed  Google Scholar 

  45. Naski MC, Wang Q, Xu J, Ornitz DM. Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat Genet. 1996;13:233–7.

    Article  CAS  PubMed  Google Scholar 

  46. Wilkes D, Rutland P, Pulleyn LJ, Reardon W, Moss C, Ellis JP, et al. A recurrent mutation, ala391glu, in the transmembrane region of FGFR3 causes Crouzon syndrome and acanthosis nigricans. J Med Genet. 1996;33:744–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Muenke M, Gripp KW, McDonald-McGinn DM, Gaudenz K, Whitaker LA, Bartlett SP, et al. A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome. Am J Hum Genet. 1997;60:555–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Makrythanasis P, Temtamy S, Aglan MS, Otaify GA, Hamamy H, Antonarakis SE. A novel homozygous mutation in FGFR3 causes tall stature, severe lateral tibial deviation, scoliosis, hearing impairment, camptodactyly, and arachnodactyly. Hum Mutat. 2014;35:959–63.

    Article  CAS  PubMed  Google Scholar 

  49. Sun X, Zhang R, Chen H, Du X, Chen S, Huang J, et al. Fgfr3 mutation disrupts chondrogenesis and bone ossification in zebrafish model mimicking CATSHL syndrome partially via enhanced Wnt/β-catenin signaling. Theranostics. 2020;10:7111–30. https://doi.org/10.7150/thno.45286. Role of FGFR3 during the viscerocranium development.

  50. Hall C, Flores MV, Murison G, Crosier K, Crosier P. An essential role for zebrafish Fgfrl1 during gill cartilage development. Mech Dev. 2006;123:925–40.

    Article  CAS  PubMed  Google Scholar 

  51. Moosa S, Wollnik B. Altered FGF signalling in congenital craniofacial and skeletal disorders. Semin Cell Dev Biol. 2016;53:115–25.

    Article  CAS  PubMed  Google Scholar 

  52. Wilkie AOM, Johnson D, Wall SA. Clinical genetics of craniosynostosis. Curr Opin Pediatr. 2017;29:622–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Meyers GA, Orlow SJ, Munro IR, Przylepa KA, Jabs EW. Fibroblast growth factor receptor 3 (FGFR3) transmembrane mutation in Crouzon syndrome with acanthosis nigricans. Nat Genet. 1995;11:462–4.

    Article  CAS  PubMed  Google Scholar 

  54. Slaney SF, Oldridge M, Hurst JA, Moriss-Kay GM, Hall CM, Poole MD, et al. Differential effects of FGFR2 mutations on syndactyly and cleft palate in Apert syndrome. Am J Hum Genet. 1996;58:923–32.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. de Planque CA, Wall SA, Dalton L, Paternoster G, Arnaud É, van Veelen M-LC, et al. Clinical signs, interventions, and treatment course of three different treatment protocols in patients with Crouzon syndrome with acanthosis nigricans. J Neurosurg Pediatr. 2021;28:425–31.

    Article  PubMed  Google Scholar 

  56. Schmetz A, Schaper J, Thelen S, Rana M, Klenzner T, Schaumann K, et al. FGF9-Associated Multiple Synostoses Syndrome Type 3 in a Multigenerational Family. Genes. 2023;14:724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Di Rocco F, Biosse Duplan M, Heuzé Y, Kaci N, Komla-Ebri D, Munnich A, et al. FGFR3 mutation causes abnormal membranous ossification in achondroplasia. Hum Mol Genet. 2014;23:2914–25.

    Article  PubMed  Google Scholar 

  58. Biosse Duplan M, Komla-Ebri D, Heuzé Y, Estibals V, Gaudas E, Kaci N, et al. Meckel’s and condylar cartilages anomalies in achondroplasia result in defective development and growth of the mandible. Hum Mol Genet. 2016;25:2997–3010.

    PubMed  PubMed Central  Google Scholar 

  59. Toydemir RM, Brassington AE, Bayrak-Toydemir P, Krakowiak PA, Jorde LB, Whitby FG, et al. A novel mutation in FGFR3 causes camptodactyly, tall stature, and hearing loss (CATSHL) syndrome. Am J Hum Genet. 2006;79:935–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Cornille M, Dambroise E, Komla-Ebri D, Kaci N, Biosse-Duplan M, Di Rocco F, et al. Animal models of craniosynostosis. Neurochirurgie. 2019;65:202–9.

    Article  CAS  PubMed  Google Scholar 

  61. Zhao X, Erhardt S, Sung K, Wang J. FGF signaling in cranial suture development and related diseases. Front Cell Dev Biol. 2023;11:1112890.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Valenti MT, Marchetto G, Mottes M, Dalle CL. Zebrafish: A Suitable Tool for the Study of Cell Signaling in Bone. Cells. 2020;9:1911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Truong BT, Artinger KB. The power of zebrafish models for understanding the co-occurrence of craniofacial and limb disorders. Genesis. 2021;59: e23407.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Li K, Fan L, Tian Y, Lou S, Li D, Ma L, et al. Application of zebrafish in the study of craniomaxillofacial developmental anomalies. Birth Defects Research. 2022;114:583–95.

    Article  CAS  PubMed  Google Scholar 

  65. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496:498–503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Duncan KM, Mukherjee K, Cornell RA, Liao EC. Zebrafish models of orofacial clefts. Dev Dyn. 2017;246:897–914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mork L, Crump G. Zebrafish Craniofacial Development: A Window into Early Patterning. Curr Top Dev Biol. 2015;115:235–69.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Choe CP, Choi S-Y, Kee Y, Kim MJ, Kim S-H, Lee Y, et al. Transgenic fluorescent zebrafish lines that have revolutionized biomedical research. Lab Anim Res. 2021;37:26. Includes list of transgenic lines for studying skeletal development.

  69. Liu K, Petree C, Requena T, Varshney P, Varshney GK. Expanding the CRISPR Toolbox in Zebrafish for Studying Development and Disease. Front Cell Dev Biol. 2019;7:13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Itoh N, Konishi M. The zebrafish fgf family. Zebrafish. 2007;4:179–86.

    Article  CAS  PubMed  Google Scholar 

  71. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov. 2009;8:235–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jen Y-HL, Musacchio M, Lander AD. Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev. 2009;4:33.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Keil S, Gupta M, Brand M, Knopf F. Heparan sulfate proteoglycan expression in the regenerating zebrafish fin. Dev Dyn. 2021;250:1368–80.

    Article  CAS  PubMed  Google Scholar 

  74. Norton WHJ, Ledin J, Grandel H, Neumann CJ. HSPG synthesis by zebrafish Ext2 and Extl3 is required for Fgf10 signalling during limb development. Development. 2005;132:4963–73.

    Article  CAS  PubMed  Google Scholar 

  75. Sugano Y, Lardelli M. Identification and expression analysis of the zebrafish orthologue of Klotho. Dev Genes Evol. 2011;221:179–86.

    Article  CAS  PubMed  Google Scholar 

  76. Mangos S, Amaral AP, Faul C, Jüppner H, Reiser J, Wolf M. Expression of fgf23 and αklotho in developing embryonic tissues and adult kidney of the zebrafish. Danio rerio Nephrol Dial Transplant. 2012;27:4314–22.

    Article  CAS  PubMed  Google Scholar 

  77. Ogura Y, Kaneko R, Ujibe K, Wakamatsu Y, Hirata H. Loss of αklotho causes reduced motor ability and short lifespan in zebrafish. Sci Rep. 2021;11:15090.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Singh AP, Sosa MX, Fang J, Shanmukhappa SK, Hubaud A, Fawcett CH, et al. αKlotho Regulates Age-Associated Vascular Calcification and Lifespan in Zebrafish. Cell Rep. 2019;28:2767-2776.e5.

    Article  CAS  PubMed  Google Scholar 

  79. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 2005;16:139–49.

    Article  CAS  PubMed  Google Scholar 

  80. Piotrowski T, Schilling TF, Brand M, Jiang Y-J, Heisenberg C-P, Beuchle D, et al. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development. 1996;123:345–56.

    Article  CAS  PubMed  Google Scholar 

  81. Schilling TF, Piotrowski T, Grandel H, Brand M, Heisenberg CP, Jiang YJ, et al. Jaw and branchial arch mutants in zebrafish I: branchial arches. Development. 1996;123:329–44.

    Article  CAS  PubMed  Google Scholar 

  82. Keer S, Cohen K, May C, Hu Y, McMenamin S, Hernandez LP. Anatomical Assessment of the Adult Skeleton of Zebrafish Reared Under Different Thyroid Hormone Profiles. Anat Rec. 2019;302:1754–69.

    Article  CAS  Google Scholar 

  83. Cubbage CC, Mabee PM. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J Morphol. 1996;229:121–60.

    Article  PubMed  Google Scholar 

  84. Weigele J, Franz-Odendaal TA. Functional bone histology of zebrafish reveals two types of endochondral ossification, different types of osteoblast clusters and a new bone type. J Anat. 2016;229:92–103.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Schilling TF, Kimmel CB. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development. 1994;120:483–94.

    Article  CAS  PubMed  Google Scholar 

  86. Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, Fisher S. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE. 2012;7: e47394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Araya C, Ward LC, Girdler GC, Miranda M. Coordinating cell and tissue behavior during zebrafish neural tube morphogenesis. Dev Dyn. 2016;245:197–208.

    Article  PubMed  Google Scholar 

  88. Köntges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996;122:3229–42.

    Article  PubMed  Google Scholar 

  89. Jovelin R, Yan Y, He X, Catchen J, Amores A, Canestro C, et al. Evolution of developmental regulation in the vertebrate FgfD subfamily. J Exp Zool Pt B. 2010;314B:33–56.

    Article  CAS  Google Scholar 

  90. Okada K, Takada S. The second pharyngeal pouch is generated by dynamic remodeling of endodermal epithelium in zebrafish. Development. 2020;147:dev194738.

    Article  CAS  PubMed  Google Scholar 

  91. Kimmel CB, Miller CT, Moens CB. Specification and Morphogenesis of the Zebrafish Larval Head Skeleton. Dev Biol. 2001;233:239–57.

    Article  CAS  PubMed  Google Scholar 

  92. Leerberg DM, Hopton RE, Draper BW. Fibroblast Growth Factor Receptors Function Redundantly During Zebrafish Embryonic Development. Genetics. 2019;212:1301–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Gebuijs L, Wagener FA, Zethof J, Carels CE, Von Den Hoff JW, Metz JR. Targeting fibroblast growth factor receptors causes severe craniofacial malformations in zebrafish larvae. PeerJ. 2022;10:e14338. https://doi.org/10.7717/peerj.14338. Studies of the simple, double and triple CrisPR/Cas9 lof fgfrs zebrafish.

  94. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA. 1998;95:5082–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994;8:3045–57.

    Article  CAS  PubMed  Google Scholar 

  96. Reifers F, Walsh EC, Léger S, Stainier DY, Brand M. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development. 2000;127:225–35.

    Article  CAS  PubMed  Google Scholar 

  97. Walshe J, Mason I. Fgf signalling is required for formation of cartilage in the head. Dev Biol. 2003;264:522–36.

    Article  CAS  PubMed  Google Scholar 

  98. Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development. 2004;131:5703–16.

    Article  CAS  PubMed  Google Scholar 

  99. Vitelli F. Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum Mol Genet. 2002;11:915–22.

    Article  CAS  PubMed  Google Scholar 

  100. Liu Y-H, Lin T-C, Hwang S-PL. Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development. Mechanisms of Development. 2020;161:103598. https://doi.org/10.1016/j.mod.2020.103598. FGF signaling and pharyngeal pouches.

  101. Blentic A, Tandon P, Payton S, Walshe J, Carney T, Kelsh RN, et al. The emergence of ectomesenchyme. Dev Dyn. 2008;237:592–601.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Yang S, Xu X, Yin Z, Liu Y, Wang H, Guo J, et al. nkx2.3 is responsible for posterior pharyngeal cartilage formation by inhibiting Fgf signaling. Heliyon. 2023;9:e21915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Heubel BP, Bredesen CA, Schilling TF, Le Pabic P. Endochondral growth zone pattern and activity in the zebrafish pharyngeal skeleton. Developmental Dynamics. 2021;250:74–87. https://doi.org/10.1002/dvdy.241. Endochondral ossification in zebrafish.

  104. Le Pabic P, Dranow DB, Hoyle DJ, Schilling TF. Zebrafish endochondral growth zones as they relate to human bone size, shape and disease. Front Endocrinol. 2022;13:1060187. https://doi.org/10.3389/fendo.2022.1060187. Review on New data regarding endochondral ossification in zebrafish.

  105. Giffin JL, Gaitor D, Franz-Odendaal TA. The Forgotten Skeletogenic Condensations: A Comparison of Early Skeletal Development Amongst Vertebrates. JDB. 2019;7:4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Sperber SM, Dawid IB. barx1 is necessary for ectomesenchyme proliferation and osteochondroprogenitor condensation in the zebrafish pharyngeal arches. Dev Biol. 2008;321:101–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Klüver N, Kondo M, Herpin A, Mitani H, Schartl M. Divergent expression patterns of Sox9 duplicates in teleosts indicate a lineage specific subfunctionalization. Dev Genes Evol. 2005;215:297–305.

    Article  PubMed  Google Scholar 

  108. Yan Y-L, Willoughby J, Liu D, Crump JG, Wilson C, Miller CT, et al. A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development. 2005;132:1069–83.

    Article  CAS  PubMed  Google Scholar 

  109. Giovannone D, Paul S, Schindler S, Arata C, Farmer DT, Patel P, et al. Programmed conversion of hypertrophic chondrocytes into osteoblasts and marrow adipocytes within zebrafish bones. eLife. 2019;8:42736.

    Article  CAS  Google Scholar 

  110. McCarthy N, Sidik A, Bertrand JY, Eberhart JK. An Fgf-Shh signaling hierarchy regulates early specification of the zebrafish skull. Dev Biol. 2016;415:261–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Niu X, Zhang F, Ping L, Wang Y, Zhang B, Wang J, et al. vwa1 Knockout in Zebrafish Causes Abnormal Craniofacial Chondrogenesis by Regulating FGF Pathway. Genes. 2023;14:838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Dash S, Trainor PA. Nucleolin loss of function leads to aberrant Fibroblast Growth Factor signaling and craniofacial anomalies. Development. 2022;149:dev200349. https://doi.org/10.1242/dev.200349. Regulation of fgf8 expression during chondrogenesis.

  113. Ornitz DM, Legeai-Mallet L. Achondroplasia: Development, Pathogenesis, and Therapy. Dev Dyn. 2016 https://doi.org/10.1002/dvdy.24479.

  114. Trueb B, Taeschler S. Expression of FGFRL1, a novel fibroblast growth factor receptor, during embryonic development. Int J Mol Med. 2006;17:617–20.

    CAS  PubMed  Google Scholar 

  115. Kanther M, Scalici A, Rashid A, Miao K, Van Deventer E, Fisher S. Initiation and early growth of the skull vault in zebrafish. Mech Dev. 2019;103578. https://doi.org/10.1016/j.mod.2019.103578.

  116. Li N, Felber K, Elks P, Croucher P, Roehl HH. Tracking gene expression during zebrafish osteoblast differentiation. Dev Dyn. 2009;238:459–66.

    Article  CAS  PubMed  Google Scholar 

  117. Kim Y-I, Lee S, Jung S-H, Kim H-T, Choi J-H, Lee M-S, et al. Establishment of a Bone-Specific col10a1:GFP Transgenic Zebrafish. Mol Cells. 2013;36:145–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Behr B, Longaker MT, Quarto N. Craniosynostosis of coronal suture in twist1 mice occurs through endochondral ossification recapitulating the physiological closure of posterior frontal suture. Front Physiol. 2011;2:37.

    Article  PubMed  PubMed Central  Google Scholar 

  119. Mitchell LA, Kitley CA, Armitage TL, Krasnokutsky MV, Rooks VJ. Normal Sagittal and Coronal Suture Widths by Using CT Imaging. AJNR Am J Neuroradiol. 2011;32:1801–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Aldawood ZA, Mancinelli L, Geng X, Yeh S-CA, Di Carlo R, Leite CT, et al. Expansion of the sagittal suture induces proliferation of skeletal stem cells and sustains endogenous calvarial bone regeneration. Proc Natl Acad Sci U S A. 2023;120:e2120826120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Debnath S, Yallowitz AR, McCormick J, Lalani S, Zhang T, Xu R, et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature. 2018;562:133–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Wilk K, Yeh S-CA, Mortensen LJ, Ghaffarigarakani S, Lombardo CM, Bassir SH, et al. Postnatal Calvarial Skeletal Stem Cells Expressing PRX1 Reside Exclusively in the Calvarial Sutures and Are Required for Bone Regeneration. Stem Cell Reports. 2017;8:933–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Zhao H, Feng J, Ho T-V, Grimes W, Urata M, Chai Y. The suture provides a niche for mesenchymal stem cells of craniofacial bones. Nat Cell Biol. 2015;17:386–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Teng CS, Ting M-C, Farmer DT, Brockop M, Maxson RE, Crump JG. Altered bone growth dynamics prefigure craniosynostosis in a zebrafish model of Saethre-Chotzen syndrome. Elife. 2018;7: e37024.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Blümel R, Zink M, Klopocki E, Liedtke D. On the traces of tcf12: Investigation of the gene expression pattern during development and cranial suture patterning in zebrafish (Danio rerio). PLoS ONE. 2019;14: e0218286.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Grova M, Lo DD, Montoro D, Hyun JS, Chung MT, Wan DC, et al. Models of cranial suture biology. J Craniofac Surg. 2012;23:1954–8.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Kague E, Roy P, Asselin G, Hu G, Simonet J, Stanley A, et al. Osterix/Sp7 limits cranial bone initiation sites and is required for formation of sutures. Dev Biol. 2016;413:160–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Laue K, Pogoda H-M, Daniel PB, van Haeringen A, Alanay Y, von Ameln S, et al. Craniosynostosis and multiple skeletal anomalies in humans and zebrafish result from a defect in the localized degradation of retinoic acid. Am J Hum Genet. 2011;89:595–606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Jeradi S, Hammerschmidt M. Retinoic acid-induced premature osteoblast-to-preosteocyte transitioning has multiple effects on calvarial development. Development. 2016;143:1205–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Tokumaru AM, Barkovich AJ, Ciricillo SF, Edwards MS. Skull base and calvarial deformities: association with intracranial changes in craniofacial syndromes. AJNR Am J Neuroradiol. 1996;17:619–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Li W, Wang M, Zhou R, Wang S, Zheng H, Liu D, et al. Exploring the interaction between FGF Genes and T-box genes among chinese nonsyndromic cleft lip with or without cleft palate case-parent trios. Environ and Mol Mutagen. 2019;60:602–6.

    Article  CAS  Google Scholar 

  132. Tan J, Jones MLM, Teague WJ, Ranjitkar S, Anderson PJ. Craniofacial anomalies in a murine model of heterozygous fibroblast growth factor 10 gene mutation. Orthod Craniofacial Res. 2024;27:84–94.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular and Physiopathological Bases of Osteochondrodysplasia, Université Paris Cité, INSERM UMR 1163, Imagine Institut, 24 boulevard Montparnasse, 75015, Paris, France

    Rachel Pereur & Emilie Dambroise

Authors
  1. Rachel Pereur
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emilie Dambroise
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

R.P. and E.D. wrote the main manuscript and prepared figure and tables. All authors reviewed the manuscript

Corresponding author

Correspondence to Emilie Dambroise.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereur, R., Dambroise, E. Insights into Craniofacial Development and Anomalies: Exploring Fgf Signaling in Zebrafish Models. Curr Osteoporos Rep (2024). https://doi.org/10.1007/s11914-024-00873-3

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11914-024-00873-3

Keywords

Search

Navigation